Disease-free monoculture farming by fungus-growing termites

Saria Otani,Michael Poulsen,Nina B Kreuzenbeck,Victoria L Challinor,Louise Lee Munk Larsen,Duur K Aanen,Christine Beemelmanns,Søren Krath Christensen,Silas Anselm Rasmussen,Sara Kildgaard

doi:10.1038/s41598-019-45364-z

Abstract

Fungus-growing termites engage in an obligate mutualistic relationship with Termitomyces fungi, which they maintain in monocultures on specialised fungus comb structures, without apparent problems with infectious diseases. While other fungi have been reported in the symbiosis, detailed comb fungal community analyses have been lacking. Here we use culture-dependent and -independent methods to characterise fungus comb mycobiotas from three fungus-growing termite species (two genera). Internal Transcribed Spacer (ITS) gene analyses using 454 pyrosequencing and Illumina MiSeq showed that non-Termitomyces fungi were essentially absent in fungus combs, and that Termitomyces fungal crops are maintained in monocultures as heterokaryons with two or three abundant ITS variants in a single fungal strain. To explore whether the essential absence of other fungi within fungus combs is potentially due to the production of antifungal metabolites by Termitomyces or comb bacteria, we performed in vitro assays and found that both Termitomyces and chemical extracts of fungus comb material can inhibit potential fungal antagonists. Chemical analyses of fungus comb material point to a highly complex metabolome, including compounds with the potential to play roles in mediating these contaminant-free farming conditions in the termite symbiosis.

Highlights

Monoculture farming faces a number of challenges, including increased susceptibility to pathogens in genetically homogenous crop populations[1,2], as exemplified by Ireland’s Great Famine caused by potato blight (Phytophthora infestans)
Our mock fungal community analyses indicated that the primers used would detect the expected range of fungi (Fig. S2), the bias towards Termitomyces might in reality be less extreme than what we observed
We evaluated the antifungal properties of extracts of comb material from six termite colonies against seven contaminants

Summary

Introduction

Monoculture farming faces a number of challenges, including increased susceptibility to pathogens in genetically homogenous crop populations[1,2], as exemplified by Ireland’s Great Famine caused by potato blight (Phytophthora infestans). While diverse crops may provide more robust defence against invasive disease[3], two major farming symbioses in nature – the New World fungus-farming ants and the Old World fungus-farming termites – maintain basidiomycete fungal crops in monoculture[4,5,6,7]. These are expected to be disease-prone because plant substrates harvested to manure the fungal crop may contain potential antagonists that could spread throughout the genetically homogeneous fungal gardens. We take a metabolomics approach to examine the fungus-comb chemical environment and test its potential for suppression of antagonists in vitro

Methods

Results

Conclusion